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Home , Forest dieback

Exploring the likelihood and mechanism of a -change-induced dieback of the Amazon

Yadvinder Malhia,1, Luiz E. O. C. Araga˜ oa, David Galbraithb, Chris Huntingfordc, Rosie Fisherd, Przemyslaw Zelazowskia, Stephen Sitche, Carol McSweeneya, and Patrick Meirb

aEnvironmental Change Institute, School of Geography and the Environment, University of Oxford, South Parks Road, Oxford OX1 3QY, United Kingdom; bSchool of GeoSciences, University of Edinburgh, Edinburgh EH8 9XP, United Kingdom; cCentre for Ecology and Hydrology, Wallingford OX10 8BB, United Kingdom; dDepartment of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, United Kingdom; and eMet Office Hadley Centre, Joint Centre for Hydro-Meteorological Research, Wallingford OX10 8BB, United Kingdom

Edited by Hans Joachim Schellnhuber, Potsdam Institute for Climate Impact Research, Potsdam, Germany, and approved December 15, 2008 (received for review June 10, 2008)

We examine the evidence for the possibility that 21st-century nonlinearities, thresholds, and feedbacks and determine which may cause a large-scale ‘‘dieback’’ or degradation components of this system are open to manipulation and man- of Amazonian rainforest. We employ a new framework for eval- agement in a manner beneficial to the long-term sustainability of uating the rainfall regime of tropical and from this deduce the Amazonian social ecological system. precipitation-based boundaries for current viability. We In this paper, we ask 3 questions. First, what are the climatic then examine climate simulations by 19 global climate models thresholds that favor the current presence of a forest as opposed (GCMs) in this context and find that most tend to underestimate to savanna? Second, what do climate models say about the likely current rainfall. GCMs also vary greatly in their projections of direction of expected climate change in Amazonia and any future climate change in Amazonia. We attempt to take into associated likelihood of large regions of Amazonia crossing account the differences between GCM-simulated and observed thresholds of forest viability during the 21st century? Third, to rainfall regimes in the 20th century. Our analysis suggests that what extent does direct human pressure (, frag- dry-season water stress is likely to increase in E. Amazonia over the mentation, and fires) influence the transition? 21st century, but the region tends toward a climate more appro- priate to seasonal forest than to savanna. These seasonal forests Current Climate and Vegetation in Amazonia may be resilient to seasonal but are likely to face inten- The lowland forests of Amazonia have a mean annual temper- sified water stress caused by higher temperatures and to be ature of 26 °C, with very little spatial variability, and a mean vulnerable to fires, which are at present naturally rare in much of annual precipitation of Ϸ2400 mm, ranging from Ͼ3000 mm in Amazonia. The spread of fire ignition associated with advancing North West Amazonia to Ͻ1500 mm at the forest–savanna deforestation, , and fragmentation may act as nucleation transition zones (5). points that trigger the transition of these seasonal forests into Two relevant features of the rainfall regime are (i) the fire-dominated, low forests. Conversely, deliberate limi- intensity and duration of the dry season and (ii) the overall water tation of deforestation and fire may be an effective intervention to supply. To describe the accumulated water stress that occurs maintain Amazonian forest resilience in the face of imposed across a dry season, we employ the maximum climatological 21st-century climate change. Such intervention may be enough to water deficit (MCWD) (6). navigate E. Amazonia away from a possible ‘‘tipping point,’’ MCWD is defined as the most negative value of climatological beyond which extensive rainforest would become unsustainable. water deficit (CWD), attained over a year, where the monthly change in water deficit is precipitation (P) (mm/month) Ϫ ͉ ͉ ͉ ͉ drought fire tropical forests adaptation evapotranspiration (E) (mm/month). For month n, ϭ ϩ Ϫ ͑ ͒ ϭ he response of components of the Earth system to increasing CWDn CWDnϪ1 Pn En; Max CWDn 0; levels of anthropogenic greenhouse-gas forcing is unlikely to T CWD ϭ CWD ; MCWD ϭ Min͑CWD ... CWD ͒ be continuous and gradual; instead there may be ‘‘tipping 0 12 1 12 elements’’ in the system (1). Among the most iconic of these is At the wettest time of the year, we assume the soil is saturated (i.e., the , with some projections suggesting the set CWD ϭ 0) and start the 12-month cycle of calculation from this possibility of substantial and rapid ‘‘dieback’’ (2–4). The Ama- wet phase. For any multiyear period, we apply this calculation to the zon forest biome is biologically the richest region on Earth, Ϸ mean annual cycle of precipitation (rather than calculating for each hosting 25% of global biodiversity, and is a major contributor year and then taking the mean MCWD). We do not attempt to to the biogeochemical functioning of the Earth system (3). Its model E but fix it at 3.33 mm/day, Ϸ100 mm/month. Hence, the large-scale degradation would leave an enduring legacy on the CWD is only an approximate indicator of actual soil water deficit functioning and diversity of the biosphere. We review the evidence for such a tipping element in Amazonia and examine projections in the context of rainforest viability Author contributions: Y.M. designed research; Y.M., L.E.O.C.A., R.F., P.Z., and S.S. per- considering direct human pressures on the forest system. formed research; Y.M., L.E.O.C.A., D.G., R.F., P.Z., and C.M. analyzed data; and Y.M., C.H., There is clear and ongoing change in the physical environment S.S., and P.M. wrote the paper. of Amazonia, whether through increasing atmospheric carbon The authors declare no conflict of interest. dioxide concentrations, associated imposed climate change, or This article is a PNAS Direct Submission. more direct intervention because of the spread of settlement, 1To whom correspondence should be addressed. E-mail: [email protected]. deforestation, forest timber extraction, or any related fire initi- This article contains supporting information online at www.pnas.org/cgi/content/full/ ation. Such perturbations are certain to persist on policy-relevant 0804619106/DCSupplemental. timescales. The challenge is to identify and characterize system © 2009 by The National Academy of Sciences of the USA

20610–20615 ͉ PNAS ͉ December 8, 2009 ͉ vol. 106 ͉ no. 49 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0804619106 Downloaded by guest on September 26, 2021 rainfall regime space defined by AP and MCWD. The analysis focuses on an area between 45°W and 70°W and 0° and 20°S, SPECIAL FEATURE covering both forest and savanna. It is evident that there are no sharp vegetation thresholds in the rainfall regime space (MCWD, AP); some savanna pixels are found in predominantly forest , and some evergreen forests are found in dry climates. The diffuseness of the boundary reflects variation in local surface hydrology and soil properties, e.g., seasonal flooding can favor savanna in dry forest climates, shallow water tables can allow gallery or riverine forest to persist in dry savanna climates, or more fertile soil may favor over grasses. The fuzziness in the thresholds may also reflect errors in vegetation or phenological classification or in the rainfall map. Nevertheless, it is possible to identify broad climatic thresholds consistent with the definition of tipping points. Evergreen forests tend to predominate if the dry season is weak (MCWD ϾϪ200 mm). If AP Ͼ 1500 mm, forests tend to predominate, intuitively becoming increasingly seasonal and decid- uous for more negative values of MCWD (the land-use classifica- Fig. 1. The relationship between vegetation type and rainfall regime. tion cannot distinguish evergreen from semideciduous forests). If Rainfall regime is derived from TRMM for the period 1998–2006. Our sug- Ͻ ϽϪ gested savanna zone is shaded (MCWD ϽϪ300 mm, AP Ͻ 1500 mm). AP 1500 mm, savannas predominate if MCWD 400 mm, and there is a broad transition zone for Ϫ400 mm Ͻ MCWD ϽϪ200 mm, where there is a gradual shift in the relative abundance of because it does not account for seasonal variation in E (driven savanna relative to forest. For analyses later in this paper, we ascribe mainly by radiation and phenology) (7) or spatial variation in E the following terms to bioclimatic spaces (not necessarily the related to soil and root properties. In addition, actual transpiration vegetation types): (i) ‘‘rainforest’’: MCWD ϾϪ200 mm; (ii) rates may increase with rising temperatures; the limitations of our ‘‘seasonal forest’’: MCWD ϽϪ200 mm and rainfall Ͼ1500 mm (the assumption of fixed E are discussed in Influences of Temperature and transition between rainforest and seasonal forest climates is in ϽϪ CO2 Change. A fixed E is also inappropriate outside of lowland reality a continuum); (iii) ‘‘savanna’’: MCWD 300 mm (mid- tropical regions, where lower energy supply may result in lower E. point of the transition range) and rainfall Ͻϭ1500 mm (latter As a metric of overall water supply, we utilize annual precipita- shaded in Fig. 1). tion (AP) (mm); for a given MCWD, higher values of AP reflect Climate and Atmospheric Change in Amazonia higher rainfall during the wet season. AP and MCWD are mapped in Fig. S1 A and B. For spatial analysis, these data are derived from Recently, temperatures in lowland tropical regions worldwide Ϸ NASA’s Tropical Rainfall Monitoring Mission (TRMM) satellite have been increasing at 0.25 °C per decade (5) and are for the period 1998–2005. TRMM has the advantage of complete projected to rise by 3–8 °C (mean 5 °C) over the 21st century coverage across otherwise data-poor areas, although it may under- under the A2 emissions scenario (Fig. S3), with the higher values estimate wet and dry extremes in rainfall (6). more likely if forest dieback induces strong local biophysical Fig. S2 plots the annual observed values of AP and MCWD for feedbacks (10). Precipitation trends are more difficult to eluci- the period 1970–1999, using the Climate Research Unit (CRU) date. There has been no overall trend in region-wide annual mean precipitation in recent decades, but evidence of increasing observational dataset (8). We employed CRU rather than frequency of dry events in southern Amazonia over the period TRMM for time series analysis and model validation because of 1970–1999 has been found (11). its longer duration. The northern and southern limits of Ama- Projections of rainfall change over the 21st century remain a zonia were approximated as 3°N and 12°S. Throughout this major challenge for climate models and, for that reason, are the paper, W. Amazonia is taken to extend from 72°W to 60°W and focus of particular scrutiny in this paper. In discussions of E. Amazonia from 60°W to 48°W. Amazonian dieback, there has been a tendency to either use one E. Amazonia is drier and more seasonal than W. Amazonia. model (2, 4, 12), perturbed physics ensembles of a single model Within E. Amazonia, in El-Nin˜o-associated dry years (e.g., 1982, (13), or to employ a number of models but without a critical 1983, and 1997) (Fig. S2), regional MCWD values approach examination of their respective outputs (2, 14). Ϫ200 mm, close to savanna transition thresholds if such dry conditions were to persist for the long term (see Hydrological Evaluating Model Projections of Rainfall Change in the 21st SCIENCE Thresholds on Current Forest Extent). In W. Amazonia, there is Century SUSTAINABILITY no or very little seasonal water stress even in dry years. This We examine all 19 models used in the Intergovernmental Panel crude East–West division masks within- region variability, e.g., on Climate Change AR4 Global Climate Models that provide SW Amazonia is as dry and seasonal as much of E. Amazonia runs over the 20th and 21st centuries under the medium-high (5). There are no significant trends in AP or MCWD during this range Special Report on Emissions Scenarios A2 (15). We period (1970–1999). examine model simulations of rainfall regime for both E. and W. Amazonia for the period 1970–1999 (‘‘the late 20th century’’) Hydrological Thresholds on Current Forest Extent and the period 2070–2099 (‘‘the late 21st century’’). Tables S1 The current biogeography of Amazonia can give some indication and S2 list the models and details of their rainfall regime. Here, of current climatic constraints on forest cover. Here, we explore none of these simulations incorporate feedbacks of vegetation these constraints by using combined satellite-derived maps of and soil change because the global is not modeled. forest extent and precipitation regime. For a vegetation cover Fig. 2A plots the late 20th-century and late 21st-century classification, we employ the Global Land Cover 2000 map (9), precipitation projections for each GCM for E. Amazonia onto distinguishing between evergreen forest, deciduous forests, the rainfall regime space (MCWD and AP) (a similar plot for W. grasslands, and shrublands (the latter two we ascribe to savanna) Amazonia is presented in Fig. S4). The mean CRU-derived Fig. S1C. Deforested areas are excluded from the analysis. rainfall regime for 1970–1999 for each region is also plotted. A Fig. 1 plots the distribution of these vegetation types in the very large variation among models is apparent, both in current

Malhi et al. PNAS ͉ December 8, 2009 ͉ vol. 106 ͉ no. 49 ͉ 20611 Downloaded by guest on September 26, 2021 where PGCM_20 and PGCM_21 are the GCM-simulated rainfall for the late 20th and 21st centuries, respectively, PCRU_20 is the observed monthly climate from the CRU climatology, and P21 is the revised estimate of rainfall for the late 21st century. The late 21st rainfall regime (MCWD and AP) is then recalculated from this revised prediction of monthly data, P21, and plotted for E. Amazonia in Fig. 2B (and for W. Amazonia in Fig. S4).Our implicit assumption is that GCM simulations better capture future seasonal changes in the relative intensity of precipitation, despite their current tendency to underestimate absolute values of precipitation. With this revised calculation, many GCMs show a strong tendency for increased seasonality over the 21st century (Fig. 2B). This tendency is driven by decreased rainfall in the dry- season period (July–October in most of Amazonia), which tends to occur irrespective of the present-day seasonality simulated by the GCM. Renormalization to observed precipitation stretches this tendency. All but 2 GCMs show more negative MCWD over the 21st century, with 10/19 models passing our approximate bioclimatic threshold from rainforest to seasonal forest (MCWD ϽϪ200 mm). However, the high value of rainfall in the observed climatology ensures that the general tendency is to- ward a seasonal forest climate rather than savanna climate; wet-season rainfall remains high enough to allow recharge of any dry-season water deficit. One model (HadCM3) dries suffi- ciently to clearly enter the savanna rainfall regime, and 4 other models approach the seasonal forest–savanna threshold. If we regard all models as independent and equally probable, we can use the fraction of models that indicate a certain result as a crude metric of probability. Hence, there is a high probability (10/19 Fig. 2. An evaluation of GCM simulations in change of rainfall regime in E. models, 53%) of transition to a rainfall regime more suitable for Amazonia. (A) The rainfall regime is simulated for the late 20th century (base of seasonal forest and a substantial probability (5/19 models, 26%) arrow) and the late 21st century (tip of arrow) for 19 GCMs under the A2 emissions of approaching a rainfall regime more appropriate for savanna. scenario. The TRMM-derived range of rainfall regime is indicated with gray pixels, These probabilities are broad indicators ascribed to rainfall the observed spatially averaged CRU climate for 1970–1999 indicated with blue stars, and the region with a suggested savanna-favoring rainfall regime is shaded. regime, not to vegetation type; how the vegetation will respond (B) The trajectories of changes in GCM rainfall regime when recalculated as to such a change in rainfall depends on multiple factors discussed relative changes forced to start from the CRU observed climatology. The tip of the under Vegetation Response to a Drying Amazon. Applying a arrow indicates the late 21st-century rainfall regime. Our suggested savanna selection criterion (MCWD ϾϪ200 mm and AP Ͼ 1500 mm, zone is shaded (MCWD ϽϪ300 mm, AP Ͻ 1500 mm). prenormalization) gives 6 models that simulate a climate regime appropriate for rainforest or seasonal forest in the late 20th century (and hence require a smaller perturbation to their climates and future trends. In E. Amazonia, almost all models simulated rainfall to match the CRU observed rainfall). Con- (18/19) substantially underestimate rainfall relative to the CRU sidering only the selected models, the decrease in MCWD over or TRMM data. In W. Amazonia, 17/19 models substantially the 21st century is still substantial but smaller, with 2 models (2/6, underestimate. The mean late 20th-century state of E. Amazonia 33%) crossing the threshold into seasonal forest and 1 model shows no substantial shift over the 21st century, although (1/6, 17%) approaching the savanna threshold. In reality, all individual models can show large shifts in either direction. models are not equivalent, and the more extreme outcomes Using the bioclimatic thresholds outlined above (MCWD Ͼ cannot be dismissed as outliers. For example, the model with the Ϫ300 mm or rainfall Ͼ1500 mm), two-thirds of the models most severe change in rainfall regime (HadCM3) captures many (13/19) fail to simulate a late 20th-century rainfall regime aspects of the coupling between Atlantic sea surface tempera- sufficient to support widespread rainforest in E. Amazonia and tures (SSTs) and Amazonian drought (12), and a different model 5/19 fail to do so in W. Amazonia. In E. Amazonia, 14/19 models weighting based on capturing interannual variability would sug- have a mean state drier than the actual Amazonian rainfall regime gest this more extreme result is more likely. in El Nin˜o years (Fig. S2). If we select only the models that simulate Why do GCMs tend to underestimate rainfall in Amazonia, a sufficient late 20th rainfall regime, again, there appears little trend and why does our analysis suggest increased seasonality over the in the mean rainfall regime over the 21st century. 21st century? The underestimation of rainfall is likely a result of The mismatch between observed climate and GCM-simulated the coarse grid scale of GCMs, resulting in poor representation climate renders the interpretation of GCM scenarios in Ama- of finer-scale meteorological processes that are known to inten- zonia challenging. For the next step of our analysis, we take the sify precipitation. Some of these features (e.g., intense localized relative change in monthly rainfall predicted by each GCM but convection in squall lines) are common to all tropical regions but offset these changes to the observed climate for the late 20th others are peculiar to South America. Many GCMs simulate that century rather than the GCM-simulated climate. For the mean the wet-season rains (the ‘‘South American monsoon’’) pene- late 21st century-rainfall in month n in GCM i: trate much further south than they actually do. In practice, their southward passage is blocked by 2 main phenomena: the high- P ͑n, i͒ Ϫ P ͑n, i͒ ͑ ͒ ϭ ͩ ϩ GCM_21 GCM_20 ͪ elevation ‘‘ventilation’’ of cool, westerly air over the Andes that P21 n, i 1 ͑ ͒ PGCM_20 n, i dissipate the convective energy of the moist Amazonian air masses and the Rossby wave-induced subsidence of air over ϫ ͑ ͒ PCRU_20 n Bolivia (16). Both of these mechanisms limit the southernly

20612 ͉ www.pnas.org͞cgi͞doi͞10.1073͞pnas.0804619106 Malhi et al. Downloaded by guest on September 26, 2021 penetration of rains and simultaneously enhance rainfall over above factors in turn, drawing on insights from field and the Amazonia convective zone. They are fundamental features experimental studies. SPECIAL FEATURE of regional atmospheric circulation that are challenging for any coarse-scale GCM to capture and are unlikely to change fun- Influences of CO2 and Temperature Change. Under the A2 emissions damentally in character over the 21st century, hence, it is likely scenario, atmospheric CO2 rises to 730-1020 ppmv by 2100 (19). the GCM underestimation of rainfall will persist into the late In addition to its greenhouse-gas role, increased CO2 will 21st-century projections. Finer-scale regional climate models potentially directly stimulate plant photosynthesis by increasing may better capture absolute rainfall. the rate of CO2 diffusion into leaves and directly enhancing the The 21st-century intensification of dry seasons suggested by rate of carboxylation (20). This may cause a transient increase in our analysis is probably partially driven by the general inten- biomass production rates and a net biomass (21), but sification of tropical circulation caused by increased temper- it may also accelerate mortality and turnover rates, leading to a atures and tropospheric moisture content (17). This intensi- more dynamic and potentially lower biomass forest. This ‘‘CO2 fication increases precipitation within the convective zone but fertilization effect’’ is likely to saturate over time because of also causes narrowing of the convective zone and suppression ecophysiological saturation, nutrient supply limitation, or eco- of convection in the neighboring air subsidence zones. Hence, logical feedbacks such as increased abundance of high turnover wet seasons intensify, but dry seasons also lengthen and (22). CO2 fertilization favors plants that utilize the C3 intensify. Therefore, MCWD becomes more negative, but AP photosynthetic pathway (most trees). However, many savanna may not necessarily decrease. In addition to this intensification grasses use instead the C4 pathway, potentially shifting the of the existing circulation, precipitation regimes are also balance in favor of forest in forest–savanna transition zones for affected by shifts in SST patterns. In particular, enhanced a given rainfall regime. Moreover, high CO2 increases water use relative warming of the tropical north Atlantic is associated efficiency (leaf stomata need to open less and allow less water to with intensification of dry seasons in S. and E. Amazonia. In escape for the same uptake of CO2), and this will partially at least one model (HadCM3), drought becomes more fre- mitigate the effect of increased dry-season intensity. quent and persistent as the northern tropical Atlantic warms In contrast, increases in atmospheric temperature will cause disproportionately over the 21st century (12). higher leaf-to-air vapor pressure deficit and thus enhance tran- We interpret our findings as suggesting that (i) there is a high spiration, causing actual soil water deficits to become increas- probability of some increase of dry-season intensity in E. Ama- ingly more severe than MCWD. Hence, even without change in zonia, with a medium probability (Ϸ30–50%) that this will result rainfall regime, warming can be expected to increase plant water in a climate more appropriate for seasonal forest; (ii) because stress (14). Increasing temperatures may also cause increases in plant metabolic activity and respiration, but it seems likely that GCMs tend to underestimate wet-season rainfall, the real-world in the longer term, these processes will acclimate to increased probability of future rainfall regimes more appropriate for temperature (23). Photosynthesis rates may reduce slightly under savanna is smaller (0–25%) but certainly not negligible; and (iii) rising temperatures because tropical forest leaves currently W. Amazonia, as a whole, is likely to stay in a rainforest-favoring operate near their temperature optimum, although this potential climate (although the drier northern and southern margins may reduction will probably be less than the concurrent gain from not), but there is a possibility (near 10%) of shifting from a higher CO concentrations (20). generally aseasonal moisture regime to a seasonally dry regime. 2 In conclusion, the 21st-century rise in CO2 may to some extent These percentage probabilities should be taken as merely indic- mitigate the effects of enhanced seasonality in rainfall and lessen ative, but our basic conclusion remains that the rainfall regime the likelihood of forest loss. However, the concurrent rise in of E. Amazonia is likely to shift over the 21st century in a temperature could increase the risk of a vegetation transition. direction that favors more seasonal forests rather than savanna. Which effect is more important? For a tentative assessment of Vegetation Response to a Drying Amazon the relative magnitude of these 2 effects, we tested the sensitivity of transpiration in the MOSES-TRIFFID vegetation model to We now consider the vegetation response to this drying: Will increases in temperature and CO2 (see SI Text and Fig. S5). The Amazonian forests simply and rapidly move to be in equilibrium imposed increases in Amazon surface temperature (ϩ4.7 °C) with any new rainfall regime, or are there additional factors to and CO2 (to 850 ppm) are typical of GCM simulations for 2100 consider? under the A2 emissions scenario. Under these conditions, and Three features make 21st century-climate change unique with adequate water supply, the model simulates the higher when compared with past climate change. (i) Any change in temperatures to increase evapotranspiration by Ϸ55%, whereas rainfall regime will occur concurrently with changes in other high CO decreases evapotranspiration by Ϸ17%. The net effect

2 SCIENCE atmospheric variables (in particular temperature and carbon is a 31% increase of evapotranspiration to 4.7 mm/day or 140 dioxide concentration) that are being pushed upwards outside of mm/month. This sensitivity analysis is tentative and warrants SUSTAINABILITY envelopes of natural variability experienced over the last tens of deeper exploration of model assumptions. Seasonally dry sys- millions of years. These variables also influence vegetation tems may limit water loss through increased stomatal closure, functioning and, thus, mediate the direct response to rainfall losing productivity to lessen water loss. The implications of such regime alone. (ii) The rates of change projected over this century an increase in evapotranspiration are 2-fold: First, the length of are rapid compared with past transitions. For instance, the the dry season (period of negative water balance) is extended, postglacial warming in Amazonia (driven predominantly by and the MCWD becomes more negative. Second, the increased by CO2 as opposed to global ice- feed- annual water demand increases the threshold annual rainfall backs) was just 0.1 °C per century (18) compared with 3–5 °C this required to maintain seasonal forest instead of savanna. In terms century. Current rates of change are so large that they are of Fig. 2B, the end point of each arrow shifts to the left, and the significant over the lifetime of individual trees, making consid- line between savanna and seasonal forest may shift upward, eration of transient responses and lags in the vegetation system though by how much also depends on other factors such as CO2 important. (iii) The atmospheric change is also accompanied by fertilization. These factors in combination would substantially an unprecedented intensity of direct pressure on the tropical increase the risk of transition from forest to savanna. forests through logging, deforestation, fragmentation, and fire use. This direct pressure is likely to influence the vulnerability or Transient Responses to Drought. We turn next to consideration of resilience of the biome to climatic change. We discuss each of the the transient response to rapid climate change. Forest trees can

Malhi et al. PNAS ͉ December 8, 2009 ͉ vol. 106 ͉ no. 49 ͉ 20613 Downloaded by guest on September 26, 2021 mortality, reducing both demographic and microclimatic ecosystem inertia.

Interaction Between Drought and Deforestation. Amazonia, and in particular its drier margins, is the scene for intense human pressure on the forest through logging, deforestation, and ex- pansion of fire use. In this context, consideration of the eco- physiological and ecological responses of the natural system to climate change gives only a partial picture of the future of Amazonia, and it is important to consider the impacts of this direct pressure and its interactions with atmospheric change. Under business-as-usual scenarios of deforestation, it is likely that significant areas of E. Amazonia would be directly defor- ested, although there remains the possibility of greatly improved governance and maintenance of forest area (2, 27). Nevertheless, it is likely that agricultural frontiers will spread further into the region, providing the threads of a web of ignition points ready to Fig. 3. Drought experiments and field observations of forest fire in the ignite Amazonian forests in the event of a shift to a drier and/or context of the mean of GCM projections in change of rainfall regime in E. and more seasonal climate (28). Pressures come from the spread of W. Amazonia. For the GCMs, the arrow base indicates late 20th-century road infrastructure through the region, coupled with increased rainfall regime whereas the arrow tip indicates late 21st-century rainfall regional and global demand for Amazonian beef and soya, and regime. For the drought experiments, the arrow base indicates control rainfall the emerging global demand for (28, 29) regime whereas the arrow tip indicates the estimated rainfall regime. Dia- This pressure will influence the response of forests in a monds indicate field studies of flammable forests (see Table S3), with rainfall number of ways by (i) directly removing forest cover and being regimes derived from TRMM (1998–2006). Our suggested savanna zone is an independent agent of Amazon dieback; (ii) directly modifying shaded (MCWD ϽϪ300 mm, AP Ͻ 1500 mm). local climate, surface temperatures, and rainfall regime, thus, contributing to regional climate change; and (iii) increasing the be long-lived organisms, and it is possible that ‘‘demographic presence of, and vulnerability to, fire. inertia’’ (inertia caused by long lifespans and slow community Deforestation may directly affect local climate by reducing local turnover) in the forest system may delay any forest dieback. recycling of soil water through deep roots into forest transpiration Moreover, the presence of forest may modify local microclimate and consequently into precipitation, although this seems to depend (evapotranspiration, rainfall generation, exclusion of invading on the scale and location of deforestation. Deforestation in E. grasses, shading of soil surface, and seedlings) sufficiently to Amazonia may reduce rainfall downwind in W. Amazonia (30), a favor the persistence of forest (‘‘microclimatic inertia’’). Once region that otherwise seems less vulnerable to change in rainfall established, closed-canopy, deep-rooted forest may persist even regime. In addition, lost forest transpiration results in decreased if the local climate has shifted to savanna conditions. A useful surface cooling and thereby an increase regional air temperatures, evaporative demand, and water stress in remaining forests. Land- analogy may be drawn from physics. In a phase transition from use change and fire also affect the rainfall regime by greatly liquid to solid, a liquid may persist in a supercooled state beyond increasing the aerosol content of the atmosphere through smoke the equilibrium threshold for solidification if there are insuffi- and dust. High aerosol content favors less frequent but more cient nucleation points (e.g., impurities) to induce solidification. intensive convective rain and possible suppression of rain in the dry By analogy, a forest may persist in the drying-induced transition season. A retreat of Amazonian forest (whether caused by defor- to savanna if there are insufficient nucleation points (most likely estation or severe drying) would therefore further exacerbate fire ignition points, see The Role of Fire, below) to break open the regional climate change by altering local water recycling and other forest and trigger the transformation. biophysical properties (10). It is conceivable that any such ecosystem inertia could be sufficient to buffer the presence of Amazonian forest into the The Role of Fire. We have argued that forests may have some 22nd century, by when, under optimistic scenarios, policy and resilience to intensification of the dry season. However, this may technological solutions may stabilize or even draw down atmo- break down when the presence of fire is considered. A number spheric CO2 concentrations. of field studies have reported that seasonal tropical forests do Two recent manipulation experiments have attempted to become temporarily flammable, but the lack of natural ignition address these questions by excluding a fraction of the incoming points in Amazonia inhibits the amount of natural fire. Fig. 3 throughfall of precipitation to the soil in 1-ha rainforest plots in plots the rainfall regime for a selection of studies that have E. Amazonia (24–26). Both experiments shifted a rainfall regime demonstrated forest flammability. Surrounding the savanna typical of evergreen forest into one near to or within the savanna bioclimate zone, there is a wider zone of potential forest bioclimatic zone (Fig. 3). These experiments induced reductions flammability where fires are possible but usually do not occur in transpiration, leaf area, reproductive output, and photosyn- because of the lack of ignition sources. However, the spread of thesis in the first 2 years (26) but there was a lag of Ϸ3 years human settlement, forest fragmentation, and logging has re- between the start of the exclusion and the onset of increased tree sulted in the expansion of ignition sources, with 28% of Brazilian mortality (25) and the beginning of the break-up of the forest Amazonia facing incipient fire pressure, now being within 10 km canopy. These experiments suggest that there may be some of an ignition source (31). The potentially critical role of fire was inherent resilience to reduced rainfall, which is linked to the apparent during recent in Amazonia, with extensive existence of deep rooting systems that can exploit substantial soil fires leaking from agricultural zones into flammable forests moisture reserves and, hence, buffer the rainforest against during the droughts of 1997, 1998, 2005, and 2007 (6, 32). seasonal drought. However, a threshold exists for rainforest Over the last decade, a number of field studies have explored the maintenance when wet-season rain does not completely recharge changes in primary exposed to individual or repeated dry-season soil-water depletion (Fig. 3). After a few years, soil fire events (33, 34). Most rainforest trees are poorly adapted to fire water reserves deplete, and the forest begins to witness enhanced stress, and even low-intensity forest can lead to extensive

20614 ͉ www.pnas.org͞cgi͞doi͞10.1073͞pnas.0804619106 Malhi et al. Downloaded by guest on September 26, 2021 tree death. These studies paint a compelling picture of how fire- such tipping point (2, 28). Recent developments in expansion of intolerant rainforests may decline and break open under scenarios protected areas, reduction of deforestation rate, and pioneering SPECIAL FEATURE of drying and increasing fire frequency, an early peek into the likely schemes for local payment for Amazonian ecosystem services ecology of an actual Amazonian dieback. They document sharply suggest that this is not impossible (2, 35). Efforts have been further increased mortality of both small and large trees, a rapid collapse bolstered by the recently stated commitment of Brazil to greatly of biomass canopy structure, a decline in large vertebrates and tree reduce net deforestation and by the inclusion of Reduced Emissions species dependent on these for dispersal, spread of fast growing, from Deforestation and Degradation (REDD) as a mechanism for wind-dispersed species more characteristic of , and mitigating climate change within United Nations climate-change accompanying substantial decline in plant and vertebrate biodiver- agreements, which greatly increases the potential funds available sity (33). for such an enterprise. Maintaining forest cover would not only be a strategy for climate-change mitigation, regional development, and Conclusion: Navigating Away from a Tipping Point? biodiversity conservation but also a potential strategy for adapta- Our analysis concluded that, under mid-high-range emissions tion as the climate of E. Amazonia tends toward one of intensified scenarios, there is a high probability of intensified dry seasons in seasonality. E. Amazonia and a medium probability that the rainfall regime The dieback of the forests of E. Amazonia in the 21st century will shift sufficiently to a climate state where seasonal forest is is far from inevitable but remains a distinct possibility. The first more viable than rainforest. Rising temperatures and transpira- priority (and ultimate responsibility) in minimizing the risk of tion rates, widespread deforestation, and climate-change- this dieback is reducing global greenhouse-gas emissions. How- induced forest retreat may further contribute to intensified ever, appropriate adaptation measures and seasonal water stress. Forests at the dry margins or on shallow with E. Amazonia could play a major role in minimizing the or infertile soils may be most vulnerable. The extent of forest prospects of large-scale while also contribut- die-back may be reduced by the ecophysiological response to ing to the global mitigation effort. Even with sufficient funds and rising CO2 concentrations and ecosystem acclimation to rising willpower, the implementation of biosphere management on temperature and possibly (temporarily) by inherent ecosystem such a scale will be a substantial challenge and understanding of the inertia in the response of forest ecosystems to climatic change. social, political, and economic context will be critically important However, the regional surface warming caused by substantial (36). The prospect of navigating much of Amazonia away from a forest loss and the rapid proliferation of human pressure points tipping point makes this a challenge worth facing up to. (in particular forest edges and fire ignition points) may substan- tially undermine this resilience. In such an event, it could be ACKNOWLEDGMENTS. We thank P. Harris, M. New, R. Betts, O. Phillips, D. considered that E. Amazonia had passed a tipping point in Cameron, and P. Brando for helpful comments. We also acknowledge the ecosystem structure and function. modeling groups, the Program for Climate Model Diagnosis and Intercom- Just as human activity and the spread of fire may be critical in parison, and the World Climate Research Programme (WCRP) Working Group on Coupled Modeling for their roles in making available the WCRP Coupled triggering a breakdown of forest resilience and consequent dieback, Model Intercomparison Project 3 multimodel dataset. Y.M. is supported by the direct intervention to maintain forest area and limit the spread of Jackson Foundation, and L.E.O.C., D.G., C.H., and R.F. are supported by the fire offers the potential to maintain forest resilience and avoid any Research Council.

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